The Plant Cell, Vol. 26: 3469, September 2014, www.plantcell.org ã 2014 American Society of Plant Biologists. All rights reserved.
IN BRIEF
A Rice KNOX Transcription Factor Represses Brassinosteroid Production in the Shoot Apical Meristem Knotted1-like homeobox (KNOX) transcription factors establish and maintain a population of self-renewing stem cells in the shoot apical meristem (SAM) of flowering plants and thereby direct aerial organ formation and determine inflorescence architecture. KNOX genes are thought to target thousands of loci; however, the relationship between KNOX and most of these loci is unknown (Bolduc et al., 2012). A growing body of evidence suggests that a major function of KNOX transcription factors is to regulate phytohormone accumulation in the SAM. Early observations that the rice KNOX gene OSH1 increases cytokinin and decreases gibberellin levels in transgenic tobacco plants prompted Kusaba et al. (1998) to hypothesize that OSH1 affects plant hormone metabolism. Subsequent studies showed that KNOX genes activate cytokinin biosynthesis (Yanai et al., 2005) and repress gibberellin production (Bolduc and Hake, 2009). In an effort to decipher KNOX regulatory networks in rice, Tsuda et al. (2014) examined the effect of altering the expression of OSH1 using an inducible OSH1 overexpressor and a loss-of-function osh1 mutant. Whereas overexpression of OSH1 caused brassinosteroid (BR) insensitivity, resulting in plants with twisted, erect leaf blades and severely shortened leaf sheaths, OSH1 loss-of-function mutants resembled BR overproducers, exhibiting increased coleoptile growth, defects in boundary formation between the SAM and first leaf primordium, and an increased lamina joint angle of the second leaf. Because brassinolide (biologically active BR) treatment greatly increased the lamina joint angle of wild-type plants, but not of plants that strongly overexpressed OSH1, the authors reasoned that OSH1 inactivates BR or inhibits BR signaling, but does not inhibit BR biosynthesis. Using chromatin immunoprecipitation sequencing (ChIP-seq) analysis, the authors
www.plantcell.org/cgi/doi/10.1105/tpc.114.131698
Silencing of BR catabolism genes in rice results in organ boundary defects. Note that the boundary between the SAM and the first leaf primordium is shallower in CYP734A2 RNA interference knockdown plants (right), in which the expression of all three CYP734A genes is reduced, than in the wild type (left). Bars ¼ 50 mm. (Adapted from Tsuda et al. [2014], Figures 6G and 6H.)
identified 4662 possible direct targets of OSH1. They found that OSH1 preferentially bound to genic regions and identified several DNA motifs that were enriched among the OSH1-bound regions. Interestingly, three BR catabolism genes (CYP734A2, CYP734A4, and CYP734A6) were rapidly upregulated upon OSH1 induction in the inducible OSH1 overexpressor plants. ChIP-quantitative PCR analysis showed that OSH1 bound to these three genes in the shoot apical meristem. An analysis of RNA interference lines in which the expression of all three CYP734A genes was reduced revealed boundary defects similar to those seen in osh1 plants (see figure) and premature differentiation of cells in the shoot apex. Finally, the authors showed that KNOX transcription factors also regulate BR-inactivating genes in maize, by ChIPseq analysis. The authors conclude that localized BR catabolism is an important regulatory step in SAM function and thereby reinforce the notion that a major function of KNOX transcription factors is to regulate hormone accumulation in the shoot apex.
Kathleen L. Farquharson Science Editor [email protected] ORCID ID: 000-0002-8032-0041 REFERENCES Bolduc, N., and Hake, S. (2009). The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 21: 1647–1658. Bolduc, N., Yilmaz, A., Mejia-Guerra, M.K., Morohashi, K., O’Connor, D., Grotewold, E., and Hake, S. (2012). Unraveling the KNOTTED1 regulatory network in maize meristems. Genes Dev. 26: 1685–1690. Kusaba, S., Kano-Murakami, Y., Matsuoka, M., Tamaoki, M., Sakamoto, T., Yamaguchi, I., and Fukumoto, M. (1998). Alteration of hormone levels in transgenic tobacco plants overexpressing the rice homeobox gene OSH1. Plant Physiol. 116: 471–476. Tsuda, K., Kurata, N., Ohyanagi, H., and Hake, S. (2014). Genome-wide study of KNOX regulatory network reveals brassinosteroid catabolic genes important for shoot meristem function in rice. Plant Cell 26: 3488–3500. Yanai, O., Shani, E., Dolezal, K., Tarkowski, P., Sablowski, R., Sandberg, G., Samach, A., and Ori, N. (2005). Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr. Biol. 15: 1566–1571.
A Rice KNOX Transcription Factor Represses Brassinosteroid Production in the Shoot Apical Meristem Kathleen L. Farquharson Plant Cell 2014;26;3469; originally published online September 16, 2014; DOI 10.1105/tpc.114.131698 This information is current as of January 3, 2015 References
This article cites 5 articles, 4 of which can be accessed free at: http://www.plantcell.org/content/26/9/3469.full.html#ref-list-1
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IN BRIEF
A Rice KNOX Transcription Factor Represses Brassinosteroid Production in the Shoot Apical Meristem Knotted1-like homeobox (KNOX) transcription factors establish and maintain a population of self-renewing stem cells in the shoot apical meristem (SAM) of flowering plants and thereby direct aerial organ formation and determine inflorescence architecture. KNOX genes are thought to target thousands of loci; however, the relationship between KNOX and most of these loci is unknown (Bolduc et al., 2012). A growing body of evidence suggests that a major function of KNOX transcription factors is to regulate phytohormone accumulation in the SAM. Early observations that the rice KNOX gene OSH1 increases cytokinin and decreases gibberellin levels in transgenic tobacco plants prompted Kusaba et al. (1998) to hypothesize that OSH1 affects plant hormone metabolism. Subsequent studies showed that KNOX genes activate cytokinin biosynthesis (Yanai et al., 2005) and repress gibberellin production (Bolduc and Hake, 2009). In an effort to decipher KNOX regulatory networks in rice, Tsuda et al. (2014) examined the effect of altering the expression of OSH1 using an inducible OSH1 overexpressor and a loss-of-function osh1 mutant. Whereas overexpression of OSH1 caused brassinosteroid (BR) insensitivity, resulting in plants with twisted, erect leaf blades and severely shortened leaf sheaths, OSH1 loss-of-function mutants resembled BR overproducers, exhibiting increased coleoptile growth, defects in boundary formation between the SAM and first leaf primordium, and an increased lamina joint angle of the second leaf. Because brassinolide (biologically active BR) treatment greatly increased the lamina joint angle of wild-type plants, but not of plants that strongly overexpressed OSH1, the authors reasoned that OSH1 inactivates BR or inhibits BR signaling, but does not inhibit BR biosynthesis. Using chromatin immunoprecipitation sequencing (ChIP-seq) analysis, the authors
www.plantcell.org/cgi/doi/10.1105/tpc.114.131698
Silencing of BR catabolism genes in rice results in organ boundary defects. Note that the boundary between the SAM and the first leaf primordium is shallower in CYP734A2 RNA interference knockdown plants (right), in which the expression of all three CYP734A genes is reduced, than in the wild type (left). Bars ¼ 50 mm. (Adapted from Tsuda et al. [2014], Figures 6G and 6H.)
identified 4662 possible direct targets of OSH1. They found that OSH1 preferentially bound to genic regions and identified several DNA motifs that were enriched among the OSH1-bound regions. Interestingly, three BR catabolism genes (CYP734A2, CYP734A4, and CYP734A6) were rapidly upregulated upon OSH1 induction in the inducible OSH1 overexpressor plants. ChIP-quantitative PCR analysis showed that OSH1 bound to these three genes in the shoot apical meristem. An analysis of RNA interference lines in which the expression of all three CYP734A genes was reduced revealed boundary defects similar to those seen in osh1 plants (see figure) and premature differentiation of cells in the shoot apex. Finally, the authors showed that KNOX transcription factors also regulate BR-inactivating genes in maize, by ChIPseq analysis. The authors conclude that localized BR catabolism is an important regulatory step in SAM function and thereby reinforce the notion that a major function of KNOX transcription factors is to regulate hormone accumulation in the shoot apex.
Kathleen L. Farquharson Science Editor [email protected] ORCID ID: 000-0002-8032-0041 REFERENCES Bolduc, N., and Hake, S. (2009). The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 21: 1647–1658. Bolduc, N., Yilmaz, A., Mejia-Guerra, M.K., Morohashi, K., O’Connor, D., Grotewold, E., and Hake, S. (2012). Unraveling the KNOTTED1 regulatory network in maize meristems. Genes Dev. 26: 1685–1690. Kusaba, S., Kano-Murakami, Y., Matsuoka, M., Tamaoki, M., Sakamoto, T., Yamaguchi, I., and Fukumoto, M. (1998). Alteration of hormone levels in transgenic tobacco plants overexpressing the rice homeobox gene OSH1. Plant Physiol. 116: 471–476. Tsuda, K., Kurata, N., Ohyanagi, H., and Hake, S. (2014). Genome-wide study of KNOX regulatory network reveals brassinosteroid catabolic genes important for shoot meristem function in rice. Plant Cell 26: 3488–3500. Yanai, O., Shani, E., Dolezal, K., Tarkowski, P., Sablowski, R., Sandberg, G., Samach, A., and Ori, N. (2005). Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr. Biol. 15: 1566–1571.
A Rice KNOX Transcription Factor Represses Brassinosteroid Production in the Shoot Apical Meristem Kathleen L. Farquharson Plant Cell 2014;26;3469; originally published online September 16, 2014; DOI 10.1105/tpc.114.131698 This information is current as of January 3, 2015 References
This article cites 5 articles, 4 of which can be accessed free at: http://www.plantcell.org/content/26/9/3469.full.html#ref-list-1
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